Abstract

Background

The process of fertilization involves a cell fusion event between the sperm and oocyte.
Although sperm contain mitochondria when they fuse with the oocyte, paternal mitochondrial
genomes do not persist in offspring and, thus, mitochondrial inheritance is maternal
in most animals. Recent evidence suggests that paternal mitochondria may be eliminated
via autophagy after fertilization. In C. elegans, sperm-specific organelles called membraneous organelles (MO) cluster together with
paternal mitochondria immediately after fertilization. These MOs but not the mitochondria
become polyubiquitinated and associated with proteasomes. The current model for the
elimination of paternal mitochondria in C. elegans is that ubiquitination of the MOs induces the formation of autophagosomes which also
capture the mitochondria and cause their degradation.

Results

Sperm-derived mitochondria and MOs show a sharp decrease in number during the time
between sperm-oocyte fusion and the onset of mitosis. During this time, paternal mitochondria
remain closely clustered with the MOs. Two types of polyubiquitin chains are observed
on the MOs: K48-linked ubiquitin chains which are known to lead to proteasomal degradation
and K63-linked ubiquitin chains which have been linked to autophagy. K48-linked ubiquitin
chains and proteasomes show up on MOs very soon after sperm-oocyte fusion. These are
present on MOs for only a short period of time. Maternal proteasomes localize to MOs
and sperm proteasomes localize to structures that are at the periphery of the MO cluster
suggesting that these two proteasome populations may have different roles in degrading
paternal material. K63-linked ubiquitin chains appear on MOs early and remain throughout
the first several cell divisions.

Conclusions

Since there are two different types of polyubiquitin chains associated with sperm
organelles and their timing differs, it suggests that ubiquitin has two or more roles
in the processing of sperm components after fertilization. The K63 chains potentially
provide a signal for autophagy of paternal organelles, whereas the K48 chains and
proteasomes may be involved in degradation of specific proteins.